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Arrested fungal biofilms as low-modulus structural bio-composites: Water holds the key

  • R. Aravinda NarayananEmail author
  • Asma Ahmed
Regular Article

Abstract.

Biofilms are self-assembling structures consisting of rigid microbial cells embedded in a soft biopolymeric extracellular matrix (ECM), and have been commonly viewed as being detrimental to health and equipment. In this work, we show that biofilms formed by a non-pathogenic fungus Neurospora discreta, are fungal bio-composites (FBCs) that can be directed to self-organize through active stresses to achieve specific properties. We induced active stresses by systematically varying the agitation rate during the growth of FBCs. By growing FBCs that are strong enough to be conventionally tensile loaded, we find that as agitation rate increases, the elongation strain at which the FBCs break, increases linearly, and their elastic modulus correspondingly decreases. Using results from microstructural imaging and thermogravimetry, we rationalize that agitation increases the production of ECM, which concomitantly increases the water content of agitated FBCs up to 250% more than un-agitated FBCs. Water held in the nanopores of the ECM acts a plasticizer and controls the ductility of FBCs in close analogy with polyelectrolyte complexes. This paradigm shift in viewing biofilms as bio-composites opens up the possibility for their use as sustainable, biodegradable, low-modulus structural materials.

Graphical abstract

Keywords

Flowing Matter: Active Fluids 

References

  1. 1.
    H.C. Flemming, J. Wingender, Nat. Rev. Microbiol. 8, 623 (2010)Google Scholar
  2. 2.
    A.P.J. Moore, D. Robson, G.D. Trinci, 21st Century Guidebook to Fungi (Cambridge University Press, Cambridge, UK, 2011)Google Scholar
  3. 3.
    J.N. Wilking, T.E. Angelini, A. Seminara, M.P. Brenner, D.A. Weitz, Mater. Res. Soc. 36, 385 (2011)Google Scholar
  4. 4.
    M.G. Mazza, J. Phys. D: Appl. Phys. 49, 203001 (2016)ADSGoogle Scholar
  5. 5.
    T. Shaw, M. Winston, C.J. Rupp, I. Klapper, P. Stoodley, Phys. Rev. Lett. 93, 98102 (2004)ADSGoogle Scholar
  6. 6.
    V.D. Gordon, M. Davis-fields, K. Kovach, J. Phys. D: Appl. Phys. 50, 223002 (2017)ADSGoogle Scholar
  7. 7.
    M. Morikawa, J. Biosci. Bioeng. 101, 1 (2006)Google Scholar
  8. 8.
    B. Li, T.J. Webster, J. Orthop. Res. 36, 22 (2018)Google Scholar
  9. 9.
    C.C.C.R. De Carvalho, Front. Mar. Sci. 5, 1 (2018)Google Scholar
  10. 10.
    N. Billings, A. Birjiniuk, T.S. Samad, P.S. Doyle, Rep. Prog. Phys. 78, 36601 (2015)Google Scholar
  11. 11.
    M. Böl, A.E. Ehret, A. Bolea Albero, J. Hellriegel, R. Krull, Crit. Rev. Biotechnol. 33, 145 (2013)Google Scholar
  12. 12.
    A. Ohashi, H. Harada, Water Sci. Technol. 29, 281 (1994)Google Scholar
  13. 13.
    P. Stoodley, R. Cargo, C.J. Rupp, S. Wilson, I. Klapper, J. Ind. Microbiol. Biotechnol. 29, 361 (2002)Google Scholar
  14. 14.
    D.N. Hohne, J.G. Younger, M.J. Solomon, Langmuir 25, 7743 (2009)Google Scholar
  15. 15.
    F. Quiles, S. Saadi, G. Francius, J. Bacharouche, F. Humbert, Biochim. Biophys. Acta 1858, 75 (2016)Google Scholar
  16. 16.
    S. Grumbein, M.W.O. Lieleg, S. Grumbein, M. Werb, J. Rheol. 60, 1085 (2016)ADSGoogle Scholar
  17. 17.
    L.I. Brugnoni, M.C. Tarifa, J.E. Lozano, D. Genovese, Biofouling 30, 1269 (2014)Google Scholar
  18. 18.
    H. Boudarel, J.D. Mathias, B. Blaysat, M. Grediac, Npj Biofilms Microbiomes 4, 17 (2018)Google Scholar
  19. 19.
    Y.I. Yaman, E. Demir, R. Vetter, A. Kocabas, Nat. Commun. 10, 2285 (2018)ADSGoogle Scholar
  20. 20.
    D.J. Wales, Energy Landscapes (Cambridge University Press, Cambridge, UK, 2003). Google Scholar
  21. 21.
    D. Needleman, Z. Dogic, Nat. Rev. Mater. 2, 17048 (2017)ADSGoogle Scholar
  22. 22.
    S. Alexander, Phys. Rep. 296, 5 (1998)Google Scholar
  23. 23.
    R. Hartmann, P.K. Singh, P. Pearce, R. Mok, B. Song, F. Díaz-Pascual, J. Dunkel, K. Drescher, Nat. Phys. 15, 251 (2019)Google Scholar
  24. 24.
    J. Garcia-Ojalvo, Nat. Phys. 15, 207 (2019)Google Scholar
  25. 25.
    K. Tai, M. Dao, S. Suresh, A. Palazoglu, C. Ortiz, Nat. Mater. 6, 454 (2007)ADSGoogle Scholar
  26. 26.
    G. Tudryn, L. Schadler, R.C. Picu, M.R. Islam, R. Bucinell, Sci. Rep. 7, 1 (2017)Google Scholar
  27. 27.
    M. Haneef, L. Ceseracciu, C. Canale, I.S. Bayer, J.A. Heredia-Guerrero, A. Athanassiou, Sci. Rep. 7, 41292 (2017)ADSGoogle Scholar
  28. 28.
    A.J.T.M. Mathijssen, F. Guzmán-Lastra, A. Kaiser, H. Löwen, Phys. Rev. Lett. 121, 248101 (2018)ADSGoogle Scholar
  29. 29.
    H.J. Vogel, Am. Nat. XCVIII, 435 (1964)Google Scholar
  30. 30.
    R. Rezakhaniha, A. Agianniotis, J.T.C. Schrauwen, A. Griffa, D. Sage, C.V.C. Bouten, F.N. Van De Vosse, M. Unser, N. Stergiopulos, Biomech. Model. Mechanobiol. 11, 461 (2012)Google Scholar
  31. 31.
    A. Heydorn, A.T. Nielsen, M. Hentzer, M. Givskov, B.K. Ersbøll, S. Molin, Microbiology 146, 2395 (2000)Google Scholar
  32. 32.
    P. Stoodley, R. Cargo, C.J. Rupp, S. Wilson, I. Klapper, J. Ind. Microbiol. Biotechnol. 29, 361 (2002)Google Scholar
  33. 33.
    W.D. Comper, R.P.W. Williams, O. Zamparo, Connect. Tissue Res. 25, 89 (1990)Google Scholar
  34. 34.
    P.S. Stewart, J. Bacteriol. 185, 1485 (2003)Google Scholar
  35. 35.
    C.P. Peter, Y. Suzuki, J. Bu, Biotechnol. Bioeng. 93, 1164 (2006)Google Scholar
  36. 36.
    P. Ghosh, J. Mondal, E. Ben-Jacob, H. Levine, Proc. Natl. Acad. Sci. U.S.A. 112, E2166 (2015)ADSGoogle Scholar
  37. 37.
    E. Paramonova, B.P. Krom, H.C. van der Mei, H.J. Busscher, P.K. Sharma, Microbiology 155, 1997 (2009)Google Scholar
  38. 38.
    H.H. Hariri, J.B. Schlenoff, Macromolecules 43, 8656 (2010)ADSGoogle Scholar
  39. 39.
    H.H. Hariri, A.M. Lehaf, J.B. Schlenoff, Macromolecules 45, 9364 (2012)ADSGoogle Scholar
  40. 40.
    D. De Beer, P. Stoodley, Z. Lewandowski, Biotechnol. Bioeng. 44, 636 (1994)Google Scholar
  41. 41.
    A. Birjiniuk, N. Billings, E. Nance, J. Hanes, K. Ribbeck, P.S. Doyle, New J. Phys. 16, 85014 (2014)Google Scholar
  42. 42.
    H.C. Flemming, J. Wingender, Nat. Rev. Microbiol. 8, 623 (2010)Google Scholar
  43. 43.
    M. Rubinstein, R.H. Colby, Polymer Physics (Oxford University Press, New York, 2003)Google Scholar
  44. 44.
    L.R. Madden, D.J. Mortisen, E.M. Sussman, S.K. Dupras, J.A. Fugate, J.L. Cuy, K.D. Hauch, M.A. Laflamme, C.E. Murry, B.D. Ratner, Proc. Natl. Acad. Sci. U.S.A. 107, 15211 (2010)ADSGoogle Scholar
  45. 45.
    A. Mohamed El-hadi, H. Alamri, Polymers 10, 1174 (2018)Google Scholar
  46. 46.
    R. Mandal, P.J. Bhuyan, P. Chaudhuri, M. Rao, C. Dasgupta, Phys. Rev. E 96, 42605 (2017)ADSGoogle Scholar

Copyright information

© EDP Sciences, Società Italiana di Fisica and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PhysicsBirla Institute of Technology and Science (Pilani)HyderabadIndia
  2. 2.School of Human and Life SciencesCanterbury Christ Church UniversityCanterburyUK

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